周偉華, 廖健祖, 3, 郭亞娟, 3, 袁翔城, 黃 暉, 劉 勝, 李 濤

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溶解有機物的光降解及其對浮游細菌和浮游植物的影響

周偉華1, 2, 廖健祖1, 2, 3, 郭亞娟1, 2, 3, 袁翔城1, 2, 黃 暉1, 2, 劉 勝1, 2, 李 濤1, 2

(1. 中國科學院南海海洋研究所熱帶海洋生物資源與生態(tài)重點實驗室, 廣東廣州510301; 2. 中國科學院海南熱帶海洋生物實驗站, 海南三亞572000; 3. 中國科學院大學, 北京100049)

作為海洋中最大的動態(tài)有機碳儲庫, 溶解有機物的光降解(主要是紫外波段)對生源要素的生物地球化學循環(huán)以及海洋生態(tài)系統(tǒng)的結構和功能具有重要的影響。本文探討了影響溶解有機物光降解的環(huán)境因素、其光化學過程和產(chǎn)物, 并重點闡述了溶解有機物的光降解對浮游細菌和浮游植物的影響。溶解有機物的來源和成分復雜, 其光降解在不同海區(qū)有不同的生態(tài)效應, 為了能更準確地把握其生態(tài)效應, 需要更全面和深入的研究。

溶解有機物; 光降解; 紫外線; 浮游細菌; 浮游植物

溶解有機物(Dissolved organic matter, DOM)是自然界中普遍存在的一類復雜的混合物。目前, 大多數(shù)的海洋DOM分離方法使用孔徑為0.7 μm的玻璃纖維膜進行過濾, 它包括通過濾膜而且之后用于實驗分析過程中不因蒸發(fā)丟失的有機物質部分, 以及在過濾過程中沒有被截留的膠體顆粒[1]。

作為海洋中最大的動態(tài)有機碳儲庫(約662 Gt碳), 海洋中DOM的生物地球化學行為對碳循環(huán)以及全球氣候變化有著重要的作用[2]。DOM根據(jù)其生物可利用性可分為: 活性DOM(Liable DOM, LDOM)、半活性DOM(Semi-Liable DOM, SLDOM)和惰性DOM(Recalcitrant DOM, RDOM)。其中RDOM的含量最高, 約占海洋DOM的95%(約624Gt碳), 與大氣中的CO2的碳量(約750 Gt碳)相當, 是一個巨大的碳匯。由于其難降解, 在海洋中有極長的停留時間, 焦念志等[3]認為RDOM是海洋重要的儲碳物質, 并提出“微型生物碳泵(Microbial carbon pump, MCP)”的概念, 即有機質在微型生物的作用下形成RDOM的過程。經(jīng)過MCP過程而形成的RDOM有較高的碳: 氮: 磷(3511: 202: 1)[4], 從而使碳以有機物的形態(tài)長期保存在海洋中, 而氮, 磷則以無機的形態(tài)被生產(chǎn)者重新吸收利用。因而, MCP不僅有儲碳的作用, 且能促進營養(yǎng)鹽的循環(huán)和生產(chǎn)力。

工業(yè)革命以來, 受人類活動的影響, 臭氧層被削薄使得更多的紫外線(Ultraviolet radiation, UV)能達到地球的表面。近年來, 甚至在一些熱帶地區(qū)也出現(xiàn)了臭氧洞, UV對水生生態(tài)系統(tǒng)的影響越來越突出, 特別是紫外線B波段(UV-B)[5-7]。Kieber等[8]在《Nature》上報道了海洋中高分子量的RDOM在紫外線作用下能發(fā)生光化學反應, 生成分子質量更小且具有生物活性的光降解產(chǎn)物, 可被浮游生物吸收利用, 從而影響海洋中碳的轉移以及浮游生物食物鏈傳遞動力學。因此, 紫外線對DOM的光降解作用可對MCP的慢速循環(huán)過程進行內容補充[3]。國內也有研究指出, DOM的光降解可以延長藍藻水華的持續(xù)時間[9]?？梢奃OM的光降解在海洋中元素的循環(huán)和海洋生態(tài)過程中均起著重要的作用。

在全球氣候變化的大環(huán)境下, 因紫外輻射的增強而導致的生態(tài)效應無疑是一個亟需研究的科學問題。生態(tài)系統(tǒng)中作為基礎生物的浮游細菌和浮游植物無疑對紫外線輻射增強引起的反應最為敏感, 為了加深了解DOM的光降解對浮游生物生態(tài)系統(tǒng)的影響, 很有必要對DOM光降解的基本過程、產(chǎn)物以及對浮游生物的影響進行詳細闡述。

1 影響DOM光降解的環(huán)境因素

由于人類活動引起的全球氣候變化(如: 紫外線增強、海水溫度升高、海洋酸化等), 使海洋生態(tài)環(huán)境遭受嚴重影響。海洋中DOM的光降解勢必也會受到這些環(huán)境因素變化的影響。1)近年來, 河口區(qū)的鐵含量呈升高的趨勢[10], 鐵含量的增加有助于DOM吸收UV, 海水pH的降低和鐵濃度增加均能提高DOM的光降解速率, 而pH的降低對DOM光降解的影響更為顯著。Molot等[11]指出: 在pH低于7時, 光降解過程主要是由羥基自由基所激發(fā)。2)在鹽度高的水體中, 陸源DOM光降解產(chǎn)生溶解無機碳(Dissolvedinorganic carbon, DIC)的速率減慢, 光漂白作用減弱[12],但光銨化以及DOM中UV254-發(fā)色團的光降解速率提升, 從而改變了DOM在光降解過程中的光吸收特性[13-14]。3)室內受控培養(yǎng)實驗表明: 在氧飽和濃度下, DOM光降解產(chǎn)生DIC的速率加快, 光漂白作用增強[15-16], 這與直接光降解過程需要氧有關[17]。4)不同波長的紫外線, 其所含的能量不同, 對DOM光降解的影響也不同。Wang等[16]報道了UV-B、UV-A和可見光三個波段對DOM光降解產(chǎn)生溶解無機物(Dissolved inorganic matter, DIM)的貢獻分別為31.8%、32.6%、25.6%。此外, 在不同季節(jié)和不同海區(qū), UV輻射強度存在很大差異, 這無疑對DOM的光降解產(chǎn)生很大的影響。5)Shirokova等[18]認為在異常高溫的水域中溶解有機碳(Dissolved organic carbon, DOC)的濃度降低了30%, 很可能是DOM光降解速率加快的緣故。Porcal等[19]探討了DOM光降解產(chǎn)生DIC的兩種可能途徑, 包括DOM直接光降解產(chǎn)生DIC以及DOM先降解產(chǎn)生顆粒有機碳(Particulate organic carbon, POC)等中間產(chǎn)物, 再降解成DIC, 前者受低溫控制, 而后者受高溫控制并起到主要作用。Ren等[20]也指出了水溫升高在很大程度上影響著DOM光降解產(chǎn)生CO的速率。此外, 海水的溫度上升還會使混合層變淺, 溫躍層更加明顯, 上下層海水垂直混合更加困難, 導致上層海水將接收更多的太陽輻射, 使得DOM光降解和光漂白將更加劇烈[21-22]。

2 DOM的主要光降解過程和產(chǎn)物

2.1 DOM的主要光降解過程

DOM的主要光降解過程可分為: 直接光降解、間接光降解和Fe3+-DOM復合物的光降解[23]。

2.1.1 直接光降解

直接光降解是一種較為簡單的光化學反應, 指的是DOM自身作為主要的發(fā)色團, 其直接吸收光而進行的化學反應, 其初級產(chǎn)物芳香性降低[24], 并能進行二次分解反應生成分子質量更小的物質[25-26]。DOM是否通過直接光降解途徑取決于DOM的化學組成及其來源。有研究指出: 陸源DOM比藻源DOM展示出更強的光反應活性, 而且陸源DOM在光降解過程中產(chǎn)生更多具有生物活性的DOC[27-28]。

2.1.2 間接光降解

間接光降解比直接光降解常見, 指的是DOM自身不能作為發(fā)色團而直接吸收光, 需要水體中存在的天然物質(如: 腐殖質或微生物等)被光激發(fā)后, 將激發(fā)態(tài)的能量轉移給化合物而導致的分解反應。其中一個重要的途徑是通過羥基自由基激發(fā)[29]。由于間接光降解能改變自然水體中阻礙光降解的化學物質的分子結構, 因此它在水體中有著特別重要的作用和意義。

2.1.3 Fe3+-DOM復合物的光降解

指的是在富含鐵元素的表層水中, Fe3+-DOM的羧酸鹽復合體通過配體到金屬的電荷轉移而形成的分解反應[27, 30]。反應包括了Fe3+到Fe2+的轉化和脫羧過程, 可見DOM光降解過程對鐵離子的氧化還原反應有重要影響[15]。

2.2 主要光解產(chǎn)物

水體中的DOM光降解改變了其原有的物理性質和化學組成, 如: 芳香性降低[31]、pH值下降[32]、疏水性[33]、吸收光譜性質[34]以及分子質量大小的改變[32]。其主要的產(chǎn)物可以分成以下3類[35]: 1)最為常見的一類產(chǎn)物就是含碳氣體, 包括: CO2、CO、CH4、DIC等[36-37]。2)低分子質量的有機化合物, 包括: 氨基酸、尿素、甲醛、乙醛、丙酮酸等[38-39]。3)氮和磷等無機鹽, 包括: NH4+、NO2–、PO43–等[40-41]。

3 DOM光降解對浮游細菌的影響

3.1 DOM光降解對浮游細菌生長的促進與抑制作用

DOM具有吸收UV的特性, 因而富含DOM的水域無疑更能阻礙UV在水層中的穿透[42]。一方面, 高濃度的DOM可以對UV敏感的浮游細菌起到保護作用; 另一方面, UV輔射引起的DOM光化學反應可產(chǎn)生活性物質, 同時光漂白作用又改變加劇了UV在水域中的穿透深度?？梢? DOM的光降解從多方面影響浮游細菌的群落結構和功能。UV促進了細菌生長的可能機制是在一定程度上, DOM光降解產(chǎn)生的活性物質在促進生長方面抵消了UV對細菌的損傷作用[8, 43]。接種在事先用UV處理過的海水中的浮游細菌可以達到更高的豐度, 表明細菌吸收利用了DOM的光化學分解產(chǎn)物[44]。在表層海水, 由于較高強度的UV輻射使得細菌活動受到嚴重的抑制, 在深5 m的表層沿岸海水, 細菌活動抑制率達到40%左右; 在貧營養(yǎng)鹽的大洋水域, 抑制作用延伸到10 m以上, 因而UV輻射使表層海水富含活性有機物質[45]。當隨著深度的增加或者通過垂直(或湍流)混合等使水層UV強度減弱, 且UV對浮游細菌的損傷由UV-A誘導的酶促反應得以修復時, 浮游細菌便能更有效地吸收光降解產(chǎn)物而得到更好的生長[44, 46]。

光化學轉化能使DOM轉化為更具活性的物質, 但也會產(chǎn)生相反的效應。研究表明, DOM光化學轉化產(chǎn)生的羰基化合物, 如: 羰酸, 成為細菌分解代謝的底物[47]。此外, DOM光降解還能產(chǎn)生具有生物活性的NH4+-N[48]。然而, Keil和Kirchman[49]發(fā)現(xiàn)DOM在太陽光的照射下, 加速了活性蛋白的“老化”, 即轉化為難降解的狀態(tài)。UV加速“老化”的報道在藻源DOM上出現(xiàn)較多, 這無疑對浮游細菌的生長起到抑制作用[50]。此外, Kramer和Herndl[51]指出浮游細菌在培養(yǎng)過程中產(chǎn)生RDOM, 這種RDOM的光降解產(chǎn)物仍然不具生物活性, 二次培養(yǎng)不會促進浮游細菌的生長。一般來說, 在呈弱酸性、離子強度和葉綠素含量低、腐殖質含量高的水域, 由UV誘導的DOM光降解對細菌的生長起促進作用[52]。

由DOM的光化學轉化造成營養(yǎng)物質結構的改變不僅影響細菌的生理功能, 還會改變細菌的群落結構[53-54]?？偟膩碚f, DOM的光降解可以改變微食物環(huán)的物質循環(huán)和能量流動, 進而影響食物鏈的結構與功能。

Chrost和Faust[55]指出在伯利茲珊瑚礁保護區(qū)中, 由于DOM光降解, 浮游細菌的生長率和二次生產(chǎn)得到提高。在北冰洋的邊緣海—波弗特海, DOM光降解產(chǎn)生的DIM可達細菌呼吸消耗量的10%, 由于冰川的融化, DOM的光降解作用將更加顯著[56]。在波羅的海, 平均每年DOC的光降解量超過了河流輸入的具有光活性的DOC量, 其中用于支持浮游細菌生物量的活性光反應產(chǎn)物占DOC光降解產(chǎn)物的20%, 表明波羅的海光降解作用是陸源DOC的匯[14]。然而, 國內雖有見對DOM與污染物、抗生素和重金屬化合物毒性的報道[57-58], 卻鮮有DOM光降解與浮游細菌耦合的報道。

3.2 DOM光降解影響浮游細菌生長的機理

由于DOM中含有光化學和生物活性成分, 光化學和生物過程對DOM的降解起到了競爭作用。Obernosterer等[28]指出了由于富含糖類物質, 藻源DOM(以培養(yǎng)過程中的產(chǎn)物為主)比陸源DOM(以腐殖質為主)更具生物活性, 而陸源DOM則含有豐富的芳香性碳, 更具光化學活性。在陸源DOM的光轉化反應過程中, 生物活性DOC含量提高了7%, 而藻源DOM沒有產(chǎn)生生物活性DOC。此外, 生物和光對DOM的降解也有互利的作用, Amado等[59]報道了在富含腐殖酸的瀉湖中, 細菌礦化作用使DOM光降解效率提高了13%, 而光降解可使細菌礦化效率提高300%。他認為在這個過程中起關鍵功能的物質為富含電子的氨基酸(如: 組氨酸、蛋氨酸、酪氨酸、色氨酸和半胱氨酸等)[60]。Amado等[60]還提出了新的模型: DOM光降解對細菌生長的影響除了與DOM的來源有關之外, 還與DOM的濃度有關。DOM在光降解過程中會產(chǎn)生一些強氧化性物質, 如: 單線態(tài)氧(Singlet oxygen), 其生成量與DOM的濃度成正相關[61-62], 而且有研究指出水域中單線態(tài)氧的含量處于被低估的狀態(tài)[63]。單線態(tài)氧可以反過來降解氨基酸和其他DOM分子, 影響DOM的組成結構并抑制細菌的生長[60-61, 64]。單線態(tài)氧對浮游細菌還有毒性作用并影響細菌代謝及其種群動力學[65]。

4 DOM光降解對浮游植物的影響

普遍認為大洋區(qū)的浮游植物初級生產(chǎn)力表現(xiàn)為氮限制, 在貧營養(yǎng)鹽的東地中海, 光銨化速率約為40 mmol/(m2·a), 與該海區(qū)大氣氮沉降量相近, 可提供新生產(chǎn)力氮需求的12%[66]。Morell和Corredor[67]發(fā)現(xiàn)近海葉綠素濃度的增加與DOM的光降解有著密切的聯(lián)系, 在富含DOM的河口區(qū), 光降解過程釋放大量的銨鹽, 為浮游植物的生長提供了豐富的無機氮, 他們估計由光銨化作用產(chǎn)生的氮鹽可達到浮游植物需氮量的50%。在波羅的海, 由RDOM光降解產(chǎn)生的生物活性氮可支持浮游植物1.2%的新生產(chǎn)力和3.6%需氮量[68]。而在智利中部上升流區(qū)的研究表明: 在春、夏季, 光銨化產(chǎn)物能支持50%~178%的浮游植物NH4+需求量[69]?？梢? DOM光降解是對海洋營養(yǎng)鹽動力學起著極其重要的作用, 特別是在貧營養(yǎng)鹽的大洋區(qū), 是海洋中的無機氮重要的來源之一。在光銨化對浮游植物生長的影響方面, 有學者[68]把波羅的海原有的浮游植物接種到DOM完全光降解的海水中培養(yǎng)發(fā)現(xiàn), 受氮限制影響的浮游植物生物量得到提高。通過模型計算得出, 夏季DOM光降解產(chǎn)生活性氮的速率為22~26 μmol/(m2·d), 使海區(qū)葉綠素含量提高12~14 μg/(m2·d)。同時, DOM的光降解產(chǎn)物DIC(CO2、HCO3–、CO32–)也可以促進浮游植物的生產(chǎn)力。當形成藻類水華時, DOM的光降解生成DIC的速率降低, 其產(chǎn)量僅能支持小于3%的生產(chǎn)力。但研究人員認為在藻華過程中產(chǎn)生的DOM(即藻源DOM)更具有光化學活性, 由于海水平流交換使外源DOM成為主要成分才導致了降解速率的降低[70]。很明顯, 這與目前的主流相悖, 因而在DOM光降解的耦合機制上還亟待更系統(tǒng)和深入的研究。此外, DOM光降解產(chǎn)生的活性氧產(chǎn)物也會對浮游植物產(chǎn)生損傷作用[71]。

近年來, 有害藻華、底層缺氧等水域生態(tài)災害頻繁發(fā)生, 嚴重地影響水域生態(tài)系統(tǒng)結構的穩(wěn)定性, 污染水域環(huán)境, 最終危害人類健康。長期以來, 人類活動所造成的水體富營養(yǎng)化被認為是引起藍藻水華的最主要因素。而且, 由于水溫上升導致的躍層的擴大、風速的減弱、光照強度和時間的增加均有助于藍藻水華的爆發(fā)[72]。有研究指出, DOM的光降解也會延長藍藻水華的持續(xù)時間[9]。一方面, 相對于其他藻類, 藍藻對于太陽光輻射具有更強的耐受性[73], 另一方面, 在適應不斷惡化的生態(tài)環(huán)境過程中, 藍藻已形成一定的自我保護機制, 如: 遷移到更深的水層避開高強度的輻射[74]; 超氧化物歧化酶(Superoxide Dismutase, SOD)、過氧化氫酶(Catalase, CAT)等抗氧化機制清除細胞內的過氧化合物[75-76]; 合成細胞外多糖[77]; 分泌具有吸收UV作用的化學物質, 如: 類菌胞素氨基酸(Mycosporine-like amino acids, MAAs)[78-79]以及偽枝藻素(Scytonemin, SCY)[80]; 通過修復和更新?lián)p傷的DNA和蛋白質, 如: 切除修復[81-82]、SOS反應[83]、光合系統(tǒng)II(PSII)蛋白的重新合成[84]; 通過細胞凋亡清除損傷嚴重的細胞[85]等。

5 DOM光降解對食物網(wǎng)的影響

浮游植物和浮游細菌作為海洋生態(tài)系統(tǒng)中的主要生產(chǎn)者和分解者, DOM光降解對其生物量和群落產(chǎn)生的變化必然會通過食物網(wǎng)傳遞影響上級營養(yǎng)級。這方面的研究報道先見于湖泊, De Lange等[86]通過培養(yǎng)實驗表明: 由紫外線造成的DOC光降解提高了微食物環(huán)中浮游細菌、低級的異養(yǎng)以及兼養(yǎng)生物的生物量。但其用于培養(yǎng)實驗的浮游生物來源于實驗室, 因此不能很好地指示自然環(huán)境狀態(tài)。Daniel等[87]研究了湖泊DOM光降解產(chǎn)物對異養(yǎng)微食物環(huán)的影響, 其研究發(fā)現(xiàn)DOM光降解提高了湖泊中總的浮游細菌、原生以及后生浮游動物的生物量。對于富營養(yǎng)鹽的水體, DOM光降解沒有引起明顯的群落變化, 但對于腐殖質水體, 鞭毛蟲、輪蟲、無節(jié)幼體以及枝角類的生物量有顯著提高。而在海洋方面的報道, V?h?talo等[88]研究了波羅的海近岸海域DOM光降解對浮游細菌為起點的三個營養(yǎng)級的影響, 其研究也表明了DOM光降解的促進作用。Stepanauskas等[89]在圣華金河口三角洲的研究指出, 由于具有生物活性DOC的含量夠低, 以DOC為基礎的微食物網(wǎng)每年僅能支持小于0.6×109g C的原生動物生產(chǎn)力, 相當于17×109g C的初級生產(chǎn)力, 即使DOC的光降解使其生物活性降低40%也不會對浮游動物以及魚類的營養(yǎng)需求產(chǎn)生重要的影響。目前, 人類活動所導致的污染物質過多排放、冰川和凍土的融化、極端氣候現(xiàn)象發(fā)生頻率的升高等提高了河流和海洋中的DOM含量[90-92]。DOM光降解對水域生態(tài)系統(tǒng)功能和結構的影響將更加顯著, 特別是沿岸海域。然而, DOM光降解對浮游植物食物網(wǎng)以及更高營養(yǎng)級的影響的研究仍然很缺乏。

6 研究展望

一方面, 由于全球氣候變化和人類活動的影響, 使河流以及海洋中DOM的濃度不斷升高; 另一方面, 由于臭氧層的削薄, 使更多的紫外線能達到地球表面。紫外線使DOM發(fā)生的光降解反應在碳、磷等生源要素的生物地球化學循環(huán)以及海洋生態(tài)過程有著越來越重要的影響。國外學者在這方面開展的研究相對較多, 主要包括: DOM光降解與浮游細菌和浮游植物的耦合及其對海洋生產(chǎn)力以及微食物網(wǎng)結構的影響、DOM光降解機理和產(chǎn)物、還有在污水處理方面的應用等[93]。然而國內相關的工作較少, 多見于DOM與污染物和重金屬化合物的毒性以及陸地土壤DOM遷移、轉化方面的報道。近年來, 國內雖有對水域生態(tài)系統(tǒng)中, DOM光降解產(chǎn)物、降解速率、對藻華的影響以及利用三維熒光光譜分析手段對DOM光降解特征和動力學方面的研究[94-95], 但仍有不少問題亟待進一步研討:

(1) 由于DOM的成分復雜, 對于來源與化學組成不同的DOM, 其光降解過程不同, 產(chǎn)物也不一致。此外, DOM的光降解過程與環(huán)境因素直接相關, 而且環(huán)境因子對于DOM的光降解是聯(lián)合起作用的。因此, 需要對DOM的來源和組成成分進行分類、對影響DOM的光降解的環(huán)境因子進行整合, 篩選主要環(huán)境因子, 構建其反應過程模型。

(2) 需要針對典型海區(qū)開展DOM光降解及其生態(tài)效應研究(如: 熱帶珊瑚礁海區(qū))。DOM具有吸收UV的作用可以減輕珊瑚礁生態(tài)系統(tǒng)的環(huán)境壓力, 同時活性光降解產(chǎn)物為其帶來營養(yǎng)物質, 通過食物網(wǎng)的傳遞促進其生產(chǎn)力。DOM的光降解作用可為珊瑚礁生態(tài)系統(tǒng)“低營養(yǎng)鹽, 高生產(chǎn)力和生物多樣性”的特征研究提供新思路。

(3) 以往的研究著重于對不同來源DOM的光化學反應, 很少有考慮到水體中DOM濃度的變化。然而, 由于人類活動和全球氣候變化使淡水流域中DOM濃度升高, 進而隨著江河流入海洋, 對海洋DOM的含量和組成成分有重要影響。因此, 有必要對陸源的DOM進行精確的成分分析, 并對DOM濃度升高和光降解對水域生態(tài)系統(tǒng)的影響進行研究。

(4) 對DOM的光降解進行長期觀察和大尺度的研究, 從而更準確地把握其生態(tài)效應和對水域生態(tài)系統(tǒng)響應的預測。

[1] Hansell D A, Carlson C A. Biogeochemistry of marine dissolved organic matter[M]. San Diego: Academic Press, 2014: 23-66.

[2] Hansell D A, Carlson C A, Repeta D J, et al. Dissolved organic matter in the ocean a controversy stimulates new insights[J]. Oceanography, 2009, 22(4): 202-211.

[3] Jiao N Z, Herndl G J, Hansell D A, et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean[J]. Nature Reviews Microbiology, 2010, 8(8): 593-599.

[4] Hopkinson C S, Vallino J J. Efficient export of carbon to the deep ocean through dissolved organic matter[J]. Nature, 2005, 433(7022): 142-145.

[5] Kirchhoff V, Schuch N J, Pinheiro D K, et al. Evidence for an ozone hole perturbation at 30 degrees south[J]. Atmospheric Environment, 1996, 30(9): 1481-1488.

[6] Orce V L, Helbling E W. Latitudinal UVR-PAR measurements in Argentina: extent of the 'ozone hole'[J]. Global and Planetary Change, 1997, 15(3-4): 113-121.

[7] H?der D P, Kumar H D, Smith R C, et al. Effects on aquatic ecosystems[J]. Journal of Photochemistry and Photobiology B-Biology, 1998, 46(1-3): 53-68.

[8] Kieber D J, Mcdaniel J, Mopper K. Photochemical source of biological substrates in sea water: implications for carbon cycling [J]. Nature, 1989, 341(6243): 637-639.

[9] Xu H C, Jiang H L. UV-induced photochemical heterogeneity of dissolved and attached organic matter associated with cyanobacterial blooms in a eutrophic freshwater lake[J]. Water Research, 2013, 47(17): 6506-6515.

[10] Kritzberg E S, Ekstrom S M. Increasing iron concentrations in surface waters – a factor behind brownification?[J]. Biogeosciences, 2012, 9(4): 1465-1478.

[11] Molot L A, Hudson J J, Dillon P J, et al. Effect of pH on photo-oxidation of dissolved organic carbon by hydroxyl radicals in a coloured, softwater stream[J]. Aquatic Sciences, 2005, 67(2): 189-195.

[12] Minor E C, Pothen J, Dalzell B J, et al. Effects of salinity changes on the photodegradation and ultraviolet-visible absorbance of terrestrial dissolved organic matter[J]. Limnology and Oceanography, 2006, 51(5): 2181-2186.

[13] Yang X F, Meng F G, Huang G C, et al. Sunlight- induced changes in chromophores and fluorophores of wastewater-derived organic matter in receiving waters The role of salinity[J]. Water Research, 2014, 62: 281-292.

[14] Aarnos H, Yl?stalo P, V?h?talo A V. Seasonal phototransformation of dissolved organic matter to ammonium, dissolved inorganic carbon, and labile substrates supporting bacterial biomass across the Baltic Sea[J]. Journal of Geophysical Research, 2012, 117: G01004.

[15] Gao H Z, Zepp R G. Factors influencing photoreactions of dissolved organic matter in a coastal river of the southeastern United State s[J]. Environmental Science & Technology, 1998, 32(19): 2940-2946.

[16] Wang X J, Lou T, Xie H X. Photochemical production of dissolved inorganic carbon from suwannee river humic acid[J]. Chinese Journal of Oceanology and Limnology, 2009, 27(3): 570-573.

[17] Sulzberger B, Durisch-Kaiser E. Chemical characterization of dissolved organic matter (DOM): A prerequisite for understanding UV-induced changes of DOM absorption properties and bioavailability[J]. Aquatic Sciences, 2009, 71(2): 104-126.

[18] Shirokova L S, Pokrovsky O S, Moreva O Y, et al. Decrease of concentration and colloidal fraction of organic carbon and trace elements in response to the anomalously hot summer 2010 in a humic boreal lake[J]. Science of the Total Environment, 2013, 463: 78-90.

[19] Porcal P, Dillon P J, Molot L A. Temperature Dependence of Photodegradation of Dissolved Organic Matter to Dissolved Inorganic Carbon and Particulate Organic Carbon[J]. Plos One, 2015, 10(6): e0128884.

[20] Ren C Y, Yang G P, Lu X L. Autumn photoproduction of carbon monoxide in Jiaozhou Bay, China[J]. Journal of Ocean University of China, 2014, 13(3): 428-436.

[21] Helms J R, Stubbins A, Perdue E M, et al. Photochemical bleaching of oceanic dissolved organic matter and its effect on absorption spectral slope and fluorescence[J]. Marine Chemistry, 2013, 155: 81-91.

[22] H?der D P, Williamson C E, Wangberg S A, et al. Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors[J]. Photochemical & Photobiological Sciences, 2015, 14(1): 108-126.

[23] Zafiriou O C, Joussotdubien J, Zepp R G, et al. Photochemistry of NaturalWaters[J]. Environmental Science & Technology, 1984, 18(12): A358-A371.

[24] Minor E C, Dalzell B L, Stubbins A, et al. Evaluating the photoalteration of estuarine dissolved organic matter using direct temperature-resolved mass spectrometry and UV-visible spectroscopy[J]. Aquatic Sciences, 2007, 69(4): 440-455.

[25] Wang W, Zafiriou O C, Chan I Y, et al. Production of hydrated electrons from photoionization of dissolved organic matter in natural waters[J]. Environmental Science & Technology, 2007, 41(5): 1601-1607.

[26] Bruccoleri A, Pant B C, Sharma D K, et al. Evaluation of Primary Photoproduct Quantum Yields in Fulvic- Acid[J]. Environmental Science & Technology, 1993, 27(5): 889-894.

[27] Meunier L, Laubscher H, Hug S J, et al. Effects of size and origin of natural dissolved organic matter compounds on the redox cycling of iron in sunlit surface waters[J]. Aquatic Sciences, 2005, 67(3): 292-307.

[28] Obernosterer I, Benner R. Competition between biological and photochemical processes in the mineralization of dissolved organic carbon[J]. Limnology and Oceanography, 2004, 49(1): 117-124.

[29] Pullin M J, Bertilsson S, Goldstone J V, et al. Effects of sunlight and hydroxyl radical on dissolved organic matter: Bacterial growth efficiency and production of carboxylic acids and other substrates[J]. Limnology and Oceanography, 2004, 49(6): 2011-2022.

[30] Voelker B M, Morel F M M, Sulzberger B. Iron redox cycling in surface waters: Effects of humic substances and light[J]. Environmental Science & Technology, 1997, 31(4): 1004-1011.

[31] V?h?talo A V, Salonen K, Salkinoja-Salonen M, et al. Photochemical mineralization of synthetic lignin in lake water indicates enhanced turnover of aromatic organic matter under solar radiation[J]. Biodegradation, 1999, 10(6): 415-420.

[32] Lou T, Xie H X, Chen G H, et al. Effects of photodegradation of dissolved organic matter on the binding of benzo (a) pyrene[J]. Chemosphere, 2006, 64(7): 1204- 1211.

[33] Choi K, Ueki M, Imai A, et al. Photoalteration of dissolved organic matter (DOM) released from Microcystis aeruginosa in different growth phases: DOM- fraction distribution and biodegradability[J]. Archiv Fur Hydrobiologie, 2004, 159(2): 271-286.

[34] Zhang Y L, Liu M L, Qin B Q, et al. Photochemical degradation of chromophoric-dissolved organic matter exposed to simulated UV-B and natural solar radiation[J]. Hydrobiologia, 2009, 627(1): 159-168.

[35] Moran M A, Zepp R G. Role of photoreactions in the formation of biologically labile compounds from dissolved organic matter[J]. Limnology and Oceanography, 1997, 42(6): 1307-1316.

[36] Guo W, Yang L, Yu X, et al. Photo-production of dissolved inorganic carbon from dissolved organic matter in contrasting coastal waters in the southwestern Taiwan Strait, China[J]. Journal of Environmental Sciences, 2012, 24(7): 1181-1188.

[37] Valentine R L, Zepp R G. Formation of Carbon Monoxide from the Photodegradation of Terrestrial Dissolved Organic Carbon in Natural Waters[J]. Environmental Science & Technology, 1993, 27(2): 409- 412.

[38] Buffam I, Mcglathery K J. Effect of ultraviolet light on dissolved nitrogen transformations in coastal lagoon water[J]. Limnology and Oceanography, 2003, 48(2): 723-734.

[39] Kieber R J, Zhou X L, Mopper K. Formation of Carbonyl Compounds from UV-Induced Photodegradation of Humic Substances in Natural Waters: Fate of Riverine Carbon in the Sea[J]. Limnology and Oceanography, 1990, 35(7): 1503-1515.

[40] Stedmon C A, Markager S, Tranvik L, et al. Photochemical production of ammonium and transformation of dissolved organic matter in the Baltic Sea[J]. Marine Chemistry, 2007, 104(3-4): 227-240.

[41] Koopmans D J, Bronk D A. Photochemical production of dissolved inorganic nitrogen and primary amines from dissolved organic nitrogen in waters of two estuaries and adjacent surficial groundwaters[J]. Aquatic Microbial Ecology, 2002, 26(3): 295-304.

[42] Zhang Y L, Zhang E L, Liu M L, et al. Variation of chromophoric dissolved organic matter and possible attenuation depth of ultraviolet radiation in Yunnan Plateau lakes[J]. Limnology, 2007, 8(3): 311-319.

[43] Lindell M J, Granéli W, Tranvik L J. Enhanced Bacterial Growth in Response to Photochemical Transformation of Dissolved Organic Matter[J]. Limnology and Oceanography, 1995, 40(1): 195-199.

[44] Herndl G J, Brugger A, Hager S, et al. Role of ultraviolet-B radiation on bacterioplankton and the availability of dissolved organic matter[J]. Plant Ecology, 1997, 128(1-2): 42-51.

[45] Herndl G J, Mulle-Niklas G, Frick J. Major Role of Ultraviolet-B in Controlling Bacterioplankton Growth in the Surface Layer of the Ocean[J]. Nature, 1993, 361(6414): 717-719.

[46] Visser P M, Poos J J, Scheper B B, et al. Diurnal variations in depth profiles of UV-induced DNA damage and inhibition of bacterioplankton production in tropical coastal waters[J]. Marine Ecology Progress Series, 2002, 228: 25-33.

[47] Bertilsson S, Tranvik L J. Photochemically produced carboxylic acids as substrates for freshwater bacterioplankton[J]. Limnology and Oceanography, 1998, 43(5): 885-895.

[48] Bushaw K L, Zepp R G, Tarr M A, et al. Photochemical release of biologically available nitrogen from aquatic dissolved organic matter[J]. Nature, 1996, 381(6581): 404-407.

[49] Keil R G, Kirchman D L. Abiotic Transformation of Labile Protein to Refractory Protein in Sea Water[J]. Marine Chemistry, 1994, 45(3): 187-196.

[50] Tranvik L, Kokalj S. Decreased biodegradability of algal DOC due to interactive effects of UV radiation and humic matter[J]. Aquatic Microbial Ecology, 1998, 14(3): 301-307.

[51] Kramer G D, Herndl G J. Photo- and bioreactivity of chromophoric dissolved organic matter produced by marine bacterioplankton[J]. Aquatic Microbial Ecology, 2004, 36(3): 239-246.

[52] Tranvik L J, Olofsson H, Bertilsson S. Photochemical effects on bacterial degradation of dissolved organic matter in lake water [C]// Bell C R, Brylinski M, Johnson-Green P. Microbial Biosystems: New Frontiers, Proceedings of the 8th International Symposium on Microbial Ecology, Halifax, Canada: Atlantic Canada Society for Microbial Ecology, 2000. 193-200.

[53] Abboudi M, Jeffrey W H, Ghiglione J F, et al. Effects of photochemical transformations of dissolved organic matter on bacterial metabolism and diversity in three contrasting coastal sites in the Northwestern Mediterranean Sea during summer[J]. Microbial Ecology, 2008, 55(2): 344-357.

[54] L?nborg C, Martinez-Garcia S, Teira E, et al. Effects of the photochemical transformation of dissolved organic matter on bacterial physiology and diversity in a coastal system[J]. Estuarine Coastal and Shelf Science, 2013, 129: 11-18.

[55] Chróst R J, Faust M A. Consequences of solar radiation on bacterial secondary production and growth rates in subtropical coastal water (Atlantic Coral Reef off Belize, Central America)[J]. Aquatic Microbial Ecology, 1999, 20(1): 39-48.

[56] Bélanger S, Xie H X, Krotkov N, et al. Photomineralization of terrigenous dissolved organic matter in Arctic coastal waters from 1979 to 2003: Interannual variability and implications of climate change[J]. Global Biogeochemical Cycles, 2006, 20(4): GB4005.

[57] Wang X H, Qu R J, Wei Z B, et al. Effect of water quality on mercury toxicity to Photobacterium phosphoreum: Model development and its application in natural waters[J]. Ecotoxicology and Environmental Safety, 2014, 104: 231-238.

[58] Tai C, Li Y B, Yin Y G, et al. Methylmercury Photodegradation in Surface Water of the Florida Everglades: Importance of Dissolved Organic Matter-Methylmercury Complexation[J]. Environmental Science & Technology, 2014, 48(13): 7333-7340.

[59] Amado A M, Cotner J B, Suhett A L, et al. Contrasting interactions mediate dissolved organic matter decomposition in tropical aquatic ecosystems[J]. Aquatic Microbial Ecology, 2007, 49(1): 25-34.

[60] Amado A M, Cotner J B, Cory R M, et al. Disentangling the Interactions Between Photochemical and Bacterial Degradation of Dissolved Organic Matter: Amino Acids Play a Central Role[J]. Microbial Ecology, 2015, 69(3): 554-566.

[61] Cory R M, Mcneill K, Cotner J P, et al. Singlet Oxygen in the Coupled Photochemical and Biochemical Oxidation of Dissolved Organic Matter[J]. Environmental Science & Technology, 2010, 44(10): 3683-3689.

[62] Cory R M, Cotner J B, Mcneill K. Quantifying Interactions between Singlet Oxygen and Aquatic Fulvic Acids[J]. Environmental Science & Technology, 2009, 43(3): 718-723.

[63] Latch D E, Mcneill K. Microheterogeneity of singlet oxygen distributions in irradiated humic acid solutions[J]. Science, 2006, 311(5768): 1743-1747.

[64] Boreen A L, Edhlund B L, Cotner J B, et al. Indirect photodegradation of dissolved free amino acids: The contribution of singlet oxygen and the differential reactivity of DOM from various sources[J]. Environmental Science & Technology, 2008, 42(15): 5492- 5498.

[65] Glaeser S P, Grossart H P, Glaeser J. Singlet oxygen, a neglected but important environmental factor: short- term and long-term effects on bacterioplankton composition in a humic lake[J]. Environmental Microbiology, 2010, 12(12): 3124-3136.

[66] Kitidis V, Uher G, Upstill-Goddard R C, et al. Photochemical production of ammonium in the oligotrophic Cyprus Gyre (Eastern Mediterranean)[J]. Biogeosciences, 2006, 3(4): 439-449.

[67] Morell J M, Corredor J E. Photomineralization of fluorescent dissolved organic matter in the Orinoco River plume: Estimation of ammonium release[J]. Journal of Geophysical Research, 2001, 106(C8): 16807-16813.

[68] V?h?talo A V, Jarvinen M. Photochemically produced bioavailable nitrogen from biologically recalcitrant dissolved organic matter stimulates production of a nitrogen-limited microbial food web in the Baltic Sea[J]. Limnology and Oceanography, 2007, 52(1): 132-143.

[69] Rain-Franco A, Mu?oz C, Fernandez C. Ammonium production off central Chile (36 degrees S) by photodegradation of phytoplankton-derived and marine dissolved organic matter[J]. PloS One, 2014, 9(6): e100224.

[70] Johannessen S C, Pena M A, Quenneville M L. Photochemical production of carbon dioxide during a coastal phytoplankton bloom[J]. Estuarine Coastal and Shelf Science, 2007, 73(1-2): 236-242.

[71] Morris J J, Johnson Z I, Szul M J, et al. Dependence of the Cyanobacterium Prochlorococcus on Hydrogen Peroxide Scavenging Microbes for Growth at the Ocean's Surface[J]. PloS One, 2011, 6(2): e16805.

[72] Zhang M, Duan H T, Shi X L, et al. Contributions of meteorology to the phenology of cyanobacterial blooms: Implications for future climate change[J]. Water Research, 2012, 46(2): 442-452.

[73] Zhang M, Kong F X, Wu X D, et al. Different photochemical responses of phytoplankters from the large shallow Taihu Lake of subtropical China in relation to light and mixing[J]. Hydrobiologia, 2008, 603: 267-278.

[74] Bebout B M, Garcia-Pichel F. UV B-Induced Vertical Migrations of Cyanobacteria in a Microbial Mat[J]. Applied and Environmental Microbiology, 1995, 61(12): 4215-4222.

[75] Wolfe-Simon F, Grzebyk D, Schofield O, et al. The role and evolution of superoxide dismutases in algae[J]. Journal of Phycology, 2005, 41(3): 453-465.

[76] Mutsuda M, Ishikawa T, Takeda T, et al. The catalase-peroxidase of Synechococcus PCC 7942: purification, nucleotide sequence analysis and expression in Escherichia coli.[J]. Biochemical Journal, 1996, 316: 251-257.

[77] Chen L Z, Wang G H, Hong S, et al. UV-B-induced Oxidative Damage and Protective Role of Exopolysaccharides in Desert Cyanobacterium Microcoleus vaginatus[J]. Journal of Integrative Plant Biology, 2009, 51(2): 194-200.

[78] Portwich A, Garcia-Pichel F. Biosynthetic pathway of mycosporines (mycosporine-like amino acids) in the cyanobacteriumsp. strain PCC 6912[J]. Phycologia, 2003, 42(4): 384-392.

[79] Garcia-Pichel F, Wingard C E, Castenholz R W. Evidence Regarding the UV Sunscreen Role of a Mycosporine-Like Compound in the Cyanobacteriumsp.[J]. Applied and Environmental Microbiology, 1993, 59(1): 170-176.

[80] Bultel-Poncé V, Felix-Theodose F, Sarthou C, et al. New pigments from the terrestrial cyanobacteriumsp. collected on the Mitaraka inselberg, French Guyana[J]. Journal of Natural Products, 2004, 67(4): 678-681.

[81] Williams E, Lambert J, Obrien P, et al. Evidence for dark repair of far ultraviolet-light damage in the blue-green alga, Gloeocapsa alpicola[J]. Photochemistry and Photobiology, 1979, 29(3): 543-547.

[82] Mcentee K, Weinstock G M, Lehman I R. recA protein-catalyzed strand assimilation: stimulation bysingle-stranded DNA-binding protein[J]. Proceedings of the National Academy of Sciences of the United States of America, 1980, 77(2): 857-861.

[83] Li S, Xu M, Su Z. Computational analysis of LexA regulons in Cyanobacteria[J]. Bmc Genomics, 2010, 11: 527-538.

[84] Nixon P J, Michoux F, Yu J F, et al. Recent advances in understanding the assembly and repair of photosystem II[J]. Annals of Botany, 2010, 106(1): 1-16.

[85] Berman-Frank I, Bidle K D, Haramaty L, et al. The demise of the marine cyanobacterium,spp., via an autocatalyzed cell death pathway[J]. Limnology and Oceanography, 2004, 49(4): 997-1005.

[86] De Lange H J, Morris D P, Williamson C E. Solar ultraviolet photodegradation of DOC may stimulate freshwater food webs[J]. Journal of Plankton Research, 2003, 25(1): 111-117.

[87] Daniel C, Granéli W, Kritzberg E S, et al. Stimulation of metazooplankton by photochemically modified dissolved organic matter[J]. Limnology and Oceanography, 2006, 51(1): 101-108.

[88] V?h?talo A V, Aarnos H, Hoikkala L, et al. Photochemical transformation of terrestrial dissolved organic matter supports hetero- and autotrophic production in coastal waters[J]. Marine Ecology Progress Series, 2011, 423: 1-14.

[89] Stepanauskas R, Moran M A, Bergamaschi B A, et al. Sources, bioavailability, and photoreactivity of dissolved organic carbon in the Sacramento-San Joaquin River Delta[J]. Biogeochemistry, 2005, 74(2): 131-149.

[90] Larsen S, Andersen T, Hessen D O. Climate change predicted to cause severe increase of organic carbon in lakes[J]. Global Change Biology, 2011, 17(2): 1186- 1192.

[91] Wilson H F, Saiers J E, Raymond P A, et al. Hydrologic drivers and seasonality of dissolved organic carbon concentration, nitrogen content, bioavailability, and export in a forested New England Stream[J]. Ecosystems, 2013, 16(4): 604-616.

[92] Dhillon G S, Inamdar S. Extreme storms and changes in particulate and dissolved organic carbon in runoff: Entering uncharted waters?[J]. Geophysical Research Letters, 2013, 40(7): 1322-1327.

[93] Passero M L, Cragin B, Hall A R, et al. Ultraviolet radiation pre-treatment modifies dairy wastewater, improving its utility as a medium for algal cultivation[J]. Algal Research, 2014, 6: 98-110.

[94] 王福利, 郭衛(wèi)東. 秋季南海珠江口和北部灣溶解有機物的光降解[J]. 環(huán)境科學學報, 2010, 30(3): 606-613. Wang Fuli, Guo Weidong. Photodegradation of DOM in the Pearl River Estuary and the Beibu Gulf of the South China Sea in Autumn[J]. Acta Scientiae Circumstantiae, 2010, 30(3): 606-613.

[95] 陳文昭, 易月圓, 余翔翔, 等. 小球藻來源溶解有機質的光化學降解特性[J]. 環(huán)境科學學報, 2012, 32(5): 1095-1103. Chen Wenzhao, Yi Yueyuan, Yu Xiangxiang, et al. Photochemical degradation of autochthonous dissolved organic matter from the culture media ofspp.[J]. Acta Scientiae Circumstantiae, 2012, 32(5): 1095-1103.

Photodegradation of dissolved organic matter and its effect on bacterioplankton and phytoplankton

ZHOU Wei-hua1, 2, LIAO Jian-zu1, 2, 3, GUO Ya-juan1, 2, 3, YUAN Xiang-cheng1, 2, HUANG Hui1, 2, LIU Sheng1, 2, LI Tao1, 2

(1. Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China; 2. Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences, Sanya 572000, China; 3. University of Chinese Academy of Sciences, Beijing 100049, China)

As the largest dynamic reservoir of organic carbon in the ocean, photodegradation of dissolved organic matter (DOM) under ultraviolet radiation (UV) has important effects on the biogeochemical cycles of biogenic elements, as well as on the structure and function of the marine ecosystem. This article summarizes the environmental factors that affect the photodegradation processes and products of DOM. In addition, the effects of photodegradation of DOM on bacterioplankton and phytoplankton are discussed. Owing to the different sources and complex compositions of DOM, the ecological effects of photodegradation are spatially different. Hence, further comprehensive studies are crucially needed to evaluate the ecological effects of photodegradation of DOM in different sea areas.

dissolved organic matter; photodegradation; ultraviolet radiation; bacterioplankton; phytoplankton

P76

A

1000-3096(2017)02-0136-09

10.11759/hykx20151214003

2015-12-14;

2016-04-17

國家自然科學基金(No.31370500, No.40806050, No.31370499)

周偉華(1976-), 男, 浙江東陽人, 博士, 研究員, 主要從事海洋生態(tài)環(huán)境研究, 電話, 020-89023225, Email: whzhou@scsio.ac.cn

Dec. 14, 2015

[National Natural Science Foundation of China, No. 31370500, No. 40806050, No. 31370499]

(本文編輯: 康亦兼)